Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution

  1. Bayly S Wheeler
  2. Erika Anderson
  3. Christian Frøkjær-Jensen
  4. Qian Bian
  5. Erik Jorgensen
  6. Barbara J Meyer  Is a corresponding author
  1. Rhodes College, United States
  2. Howard Hughes Medical Institute, University of California, Berkeley, United States
  3. Stanford University, United States
  4. Howard Hughes Medical Institute, University of Utah, United States

Abstract

Changes in chromosome number impair fitness by disrupting the balance of gene expression. Here we analyze mechanisms to compensate for changes in gene dose that accompanied the evolution of sex chromosomes from autosomes. Using single-copy transgenes integrated throughout the Caenorhabditis elegans genome, we show that expression of all X-linked transgenes is balanced between XX hermaphrodites and XO males. However, proximity of a dosage compensation complex (DCC) binding site (rex site) is neither necessary to repress X-linked transgenes nor sufficient to repress transgenes on autosomes. Thus, X is broadly permissive for dosage compensation, and the DCC acts via a chromosome-wide mechanism to balance transcription between sexes. In contrast, no analogous X-chromosome-wide mechanism balances transcription between X and autosomes: expression of compensated hermaphrodite X-linked transgenes is half that of autosomal transgenes. Furthermore, our results argue against an X-chromosome dosage compensation model contingent upon rex-directed positioning of X relative to the nuclear periphery.

Data availability

The following previously published data sets were used

Article and author information

Author details

  1. Bayly S Wheeler

    Department of Biology, Rhodes College, Memphis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Erika Anderson

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Christian Frøkjær-Jensen

    Department of Pathology, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Qian Bian

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Erik Jorgensen

    Department of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Barbara J Meyer

    Department of Molecular and Cell Biology, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States
    For correspondence
    bjmeyer@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6530-4588

Funding

National Institutes of Health (1R01 GM030702)

  • Barbara J Meyer

Howard Hughes Medical Institute

  • Barbara J Meyer

National Institutes of Health (1F32 GM100647)

  • Bayly S Wheeler

Howard Hughes Medical Institute

  • Christian Frøkjær-Jensen

National Institutes of Health (1R01 GM095817)

  • Erik Jorgensen

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Edith Heard, Institut Curie, France

Publication history

  1. Received: April 29, 2016
  2. Accepted: August 29, 2016
  3. Accepted Manuscript published: August 30, 2016 (version 1)
  4. Accepted Manuscript updated: September 1, 2016 (version 2)
  5. Version of Record published: October 3, 2016 (version 3)

Copyright

© 2016, Wheeler et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Bayly S Wheeler
  2. Erika Anderson
  3. Christian Frøkjær-Jensen
  4. Qian Bian
  5. Erik Jorgensen
  6. Barbara J Meyer
(2016)
Chromosome-wide mechanisms to decouple gene expression from gene dose during sex-chromosome evolution
eLife 5:e17365.
https://doi.org/10.7554/eLife.17365

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